Analysis of the structure and stability of omega loop A replacements in yeast iso-1-cytochrome c

Protein Science

Volumn 6, Issue 1, 1997, Pages 197-210

  Fetrow, Jacquelyn S ^a   Horner, Scott R ^a   Oehrl, Wolf ^a   Schaak, Diane L ^a   Boose, Terry L ^a   Burton, Randall E ^a,b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

hydrophobic core packing; modular mutagenesis; omega loops; protein design; protein engineering; protein folding; protein structure

Indexed keywords

CYTOCHROME C;

ARTICLE; GENE DELETION; GENE REARRANGEMENT; GENETIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; YEAST;

EID: 0031022598     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560060122     Document Type: Article

References (77)

1. Allemann RK, Presnell SR, Benner SA. 1991. A hybrid of bovine pancreatic ribonuclease and human angiogenin: An external loop as a module controlling substrate specificity. Protein Eng 4:831-835.
2. Auld DS, Pielak GJ. 1991. Constraints on amino acid substitutions in the N-terminal helix of cytochrome c explored by random mutagenesis. Biochemistry 30:8684-8690.
3. Bai Y, Englander SW. 1996. Future directions in folding: The multi-state nature of protein structure. Proteins Struct Funct Gen 24:145-151.
4. Bai Y, Sosnick TR, Mayne L, Englander SW. 1995. Protein folding intermediates: Native-state hydrogen exchange. Science 269:192-197.
5. Baldisseri DM, Torchia DA, Poole LB, Gerlt JA. 1991. Deletion of the Ω-loop in the active site of staphylococcal nuclease. 2. Effects on protein structure and dynamics. Biochemistry 30:3628-3633.
6. Becktel WJ, Schellman JA. 1987. Protein stability curves. Biopolymers 26:1859-1877.
7. Berghuis AM, Brayer GD. 1992. Oxidation state dependent conformational changes in cytochrome c. J Mol Biol 223:959-976.
8. Berghuis AM, Guillemette JG, Smith M, Brayer GD. 1994. Mutation of tyrosine-67 to phenylalanine in cytochrome c significantly alters the local heme environment. J Mol Biol 235:1326-1341.
9. Betz S, Pielak GJ. 1992. Introduction of a disulfide bond into cytochrome c stabilizes a compact denatured state. Biochemistry 31:12337-12344.
10. Bhatia GE. 1981. Refinement of the cystal structure of oxidized Rhodospirillum rubrum cytochrome c2 [dissertation]. San Diego, California: University of California.
11. Bowler BE, May K, Zaragoza T, York P, Dong A, Caughey WS. 1993. Destabilizing effects of replacing a surface lysine of cytochrome c with aromatic amino acids: Implications for the denatured state. Biochemistry 32:183-190.
12. 2+-binding loop into subtilisin BPN. Biochemistry 31:7796-7801.
13. Bushnell GW, Louie GV, Brayer GD. 1990. High resolution three-dimensional structure of horse heart cytochrome c. J Mol Biol 214:585-595.
14. Cohen DS, Pielak GJ. 1994. Stability of yeast iso-1-ferricytochrome c-as a function of pH and temperature. Protein Sci 3:1253-1260.
15. Colón W, Elöve GA, Wakem LP, Sherman F, Roder H. 1996. Side chain packing of the N-and C-terminal helices plays a critical role in the kinetics of cytochrome c folding. Biochemistry 35:5538-5549.
16. Cottrell SF, Rabinowitz M, Getz GS. 1975. Cytochrome synthesis in synchronous cultures of the yeast, Saccharomyces cerevisiae. J Biol Chem 250:4087-4094.
17. Cutler RL, Pielak GJ, Mauk AG, Smith M. 1987. Replacement of cysteine-107 of Saccharomyces cerevisiae iso-1-cytochrome c with threonine: Improved stability of the mutant protein. Protein Eng 1:95-99.
18. ElHawrani AS, Foreton KM, Sessions RB, Clarke AR, Holbrook JJ. 1994. Engineering surface loops of proteins - A preferred strategy for obtaining new enzyme function. Trends Biotechnol 12:207-211.
19. Elöve GA, Bhuyan AK, Roder H. 1994. Kinetic mechanism of cytochrome c folding: Involvement of the heme and its ligands. Biochemistry 33:6925-6935.
20. Elwell ML, Schellman JA. 1977. Stability of phage T4 lysozymes I. Native properties and thermal stability of wild type and two mutant lysozymes. Biochim Biophys Acta 494:367-383.
21. Ernst JF, Hampsey DM, Stewart JW, Rackovsky S, Goldstein D, Sherman F. 1985. Substitutions of proline 76 in yeast iso-1-cytochrome c: Analysis of residues compatible and incompatible with folding requirements. J Biol Chem 260:13225-13236.
22. Fetrow JS. 1995. Omega loops: Nonregular secondary structures significant in protein function and stability. FASEB J 9:708-717.
23. Fetrow JS, Cardillo TS, Sherman F. 1989. Deletions and replacements of omega loops in yeast iso-1-cytochrome c. Proteins Struct Funct Genet 6:372-381.
24. Fredericks ZL, Pielak GJ. 1993. Exploring the interface between the N-and C-terminal helices of cytochrome c by random mutagenesis within the C-terminal helix. Biochemistry 32:929-936.
25. Fumo G, Spitzer JS, Fetrow JS. 1995. A method of directed random mutagenesis of the yeast chromosome shows that iso-1-cytochrome c heme ligand His 18 is essential. Gene 164:33-39.
26. Gao Y, Boyd J, Pielak GJ, Williams RJP. 1991. Comparison of reduced and oxidized yeast iso-1-cytochrome c using paramagnetic shifts. Biochemistry 30:1928-1934.
27. Gao Y, Boyd J, Williams RJP, Pielak GJ. 1990. Assignment of proton resonances, identification of secondary structural elements, and analysis of backbone chemical shifts for the C102T variant of yeast iso-1-cytochrome c and horse cytochrome c. Biochemistry 29:6994-7003.
28. Gekko K, Yamagami K, Kunori Y, Ichihara S, Kodama M, Iwakura M. 1993. Effects of point mutation in a flexible loop on the stability and enzymatic function of Escherichia coli dihydrofolate reductase. J Biochem (Tokyo) 113:74-80.
29. Hampsey DM, Das G, Sherman F. 1986. Amino acid replacements in yeast iso-1-cytochrome c. J Biol Chem 261:3259-3271.
30. Mickey DR, Berghuis AM, Lafond B, Jaeger JA, Cardillo TS, McLendon D, Das G, Sherman F, Brayer GD, McLendon G. 1991. Enhanced thermodynamic stabilities of yeast iso-1-cytochrome c with amino acid replacements at positions 52 and 102. J Biol Chem 266:11686-11694.
31. Hilgen-Willis S. 1993. [dissertation]. Chapel Hill, North Carolina: University North Carolina.
32. Hoedemaeker FJ, vanEijsden RR, Diaz CL, Depater BS, Kijne JW. 1993. Destabilization of pea lectin by substitution of a single amino acid in a surface loop. Plant Mol Biol 22:1039-1046.
33. Holzschu D, Principio L, Conklin KT, Hickey DR, Short J, Rao R, McLendon G, Sherman F. 1987. Replacement of the invariant lysine 77 by arginine in yeast iso-1-cytochrome c results in enhanced and normal activities in vitro and in vivo. J Biol Chem 262:7125-7131.
34. Hynes TR, Kautz RA, Goodman MA, Gill JF, Fox RO. 1989. Transfer of a β-turn structure to a new protein context. Nature 339:73-76.
35. Johnson WC Jr. 1990. Protein secondary structure and circular dichroism: A practical guide. Proteins Struct Funct Genet 7:205-214.
36. Jones PT, Dear PH, Foote J, Neuberger MS, Winter G. 1986. Replacing the complementarity-determining regions in human antibody with those from a mouse. Nature 321:522-525.
37. Kunkel TA, Roberts JD, Zakour RA. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol 154:367-382.
38. Leszczynski JF, Rose GD. 1986. Loops in globular proteins: A novel category of protein secondary structure. Science 234:849-855.
39. Leszczynski JSF. 1986. Loops: A novel class of protein secondary structure [dissertation]. Hershey, Pennsylvania: The Pennsylvania State University College of Medicine.
40. Li L, Falzone CJ, Wright PE, Benkovic SJ. 1992. Functional role of a mobile loop of Escherichia coli dihydrofolate reductase in transition-state stabilization. Biochemistry 31:7826-7833.
41. Linske-O'Connell LI, McLendon G, Sherman F. 1995. Site specific combinations of stabilizing and destabilizing amino acid replacements in yeast cytochrome c: In vivo and in vitro effects. Biochemistry 34:7103-7112.
42. Lo TP, Murphy MEP, Guillemette JG, Smith M, Brayer GD. 1995. Replacements in a conserved leucine cluster in the hydrophobic heme pocket of cytochrome c. Protein Sci 4:198-208.
43. Louie GV, Brayer BD. 1989. A polypeptide chain-refolding event occurs in the Gly 82 variant of yeast iso-1-cytochrome c. J Mol Biol 210:313-322.
44. Louie GV, Brayer GD. 1990. High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c. J Mol Biol 214:527-555.
45. Louie GV, Pielak GJ, Smith M, Brayer GD. 1988. The role of Phe-82 in yeast iso-1-cytochrome c and remote conformational changes induced by a serine at this position. Biochemistry 27:7870-7876.
46. Margoliash E, Frohwirt N. 1959. Spectrum of horse-heart cytochrome c. Biochem J 71:570-572.
47. Marmorino JL, Auld DS, Betz SF, Doyle DF, Young GB, Pielak GJ. 1993. Amide proton exchange rates of oxidized and reduced Saccharomyces cerevisiae iso-1-cytochrome c. Protein Sci 2:1966-1974.
48. Matthews BW, Nicholson H, Becktel WJ. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc Natl Acad Sci USA 84:6663-6667.
49. Moore GR, Pettigrew GW. 1990. Cytochromes c. Evolutionary, structural and physicochemical aspects. Berlin: Springer-Verlag.
50. Mulligan-Pullyblank P, Spitzer JS, Gilden BM, Fetrow JS. 1996. Loop replacement and random mutagenesis of omega loop D, residues 70-84, in iso-1-cytochrome c. J Biol Chem 271:8633-8645.
51. Murphy MEP, Fetrow JS, Burton RE, Brayer GD. 1993. The structure and function of omega loop A replacements in cytochrome c. Protein Sci 2:1429-1440.
52. Murphy MEP, Nall BT, Brayer GD. 1992. Structure determination and analysis of yeast iso-2-cytochrome c and a composite mutant protein. J Mol Biol 227:160-176.
53. Myer YP. 1985. Circular dichroism studies of electron-transport components. Curr Topics Bioenergetics 14:149-188.
54. Nall BT, Landers TA. 1981. Guanidine hydrochloride induced unfolding of yeast iso-2-cytochrome c. Biochemistry 20:5403-5410.
55. Nall BT, Zuniga EH. 1990. Rates and energetics of tyrosine ring flips in yeast iso-2-cytochrome c. Biochemistry 29:7576-7584.
56. Ochi H, Hata V, Tanaka N, Kakudo M, Sakurai T, Aihara S, Morita Y. 1983. Structure of rice ferricytochrome c at 2.0 angstroms resolution. J Mol Biol 166:407-418.
57. Pan QW, Tanase S, Fukumoto Y, Nagashima F, Rhee S, Rogers PH, Arnone A, Morino Y. 1993. Functional roles of valine 37 and glycine 38 in the mobile loop of porcine cytosolic aspartate aminotransferase. J Biol Chem 268:24758-24765.
58. Pelletier H, Kraut J. 1992. Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c. Science 258:1748-1755.
59. Pettigrew GW, Moore GR. 1987. Cytochromes c biological aspects. Berlin: Springer-Verlag.
60. Pielak GJ, Auld DS, Beasley JR, Betz SF, Cohen DS, Doyle DF, Finger SA, Fredericks ZL, Hilgen-Willis S, Saunders AJ, Trojak SK. 1995. Protein thermal denaturation, side-chain models, and evolution: Amino acid substitutions at a conserved helix-helix interface. Biochemistry 34:3268-3276.
61. Pielak GJ, Boyd J, Moore GR, Williams RJP. 1988. Proton-NMR studies show that the Thr-102 mutant of yeast iso-1-cytochrome c is a typical member of the eukaryotic cytochrome c family. Eur J Biochem 177:167-177.
62. Pielak GJ, Oikawa K, Mauk AG, Smith M, Kay CM. 1986. Elimination of the negative Soret cotton effect of eukaryotic cytochromes c by replacement of an invariant phenylakinine residue by site-directed mutagenesis. J Am Chem Soc 108:2124-2121.
63. Pompliano DL, Peyman A, Knowles JR. 1990. Stabilization of a reaction intermediate as a catalytic device: Definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry 29:3186-3194.
64. Poole LB, Loveys DA, Hale SP, Gerlt JA, Stanczyk SM, Bolton PH. 1991. Deletion of the Ω-loop in the active site of staphylococcal nuclease. 1. Effect on catalysis and stability. Biochemistry 30:3621-3627.
65. Ramdas L, Sherman F, Nall BT. 1986. Guanidine hydrochloride induced equilibrium unfolding of mutant forms of iso-1-cytochrome c with replacement of proline-71. Biochemistry 25:6952-6958.
66. Reidhaar-Olsen JF, Parsell DA, Sauer RT. 1990. An essential protein in lambda repressor is required for resistance to intracellular proteolysis. Biochemistry 29:7563.
67. Roder H, Elove GA, Englander SW. 1988. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335:700-704.
68. Scheerlinck JPY, Lasters I, Claessens M, DeMaeyer M, Pio F, Delhaise P, Wodak SJ. 1992. Recurrent αβ loops structures in TIM barrel motifs show a distinct pattern of conserved structural features. Proteins Struct Funct Genet 12:299-313.
69. Schweingruber ME, Sherman F, Stewart JW. 1977. Altered absorption spectra of iso-1-cytochrome c from mutants of yeast. J Biol Chem 252:6577-6580.
70. Sherman F, Slonimski PP. 1964. Respiration-deficient mutants of yeast. II. Biochemistry. Biochim Biophys Acta 90:1-15.
71. Sherman F, Stewart JW, Jackson M, Gilmore RA, Parker JH. 1974. Mutants of yeast defective in iso-1-cytochrome c. Genetics 77:255-284.
72. Sherman F, Stewart JW, Parker JH, Inhaber E, Shipman NA, Putterman GJ, Gardishy RL, Margoliash E. 1968. The mutational alteration of the primary structure of yeast iso-1-cytochrome c. J Biol Chem 243:5446-5456.
73. Takano T, Dickerson RE. 1980. Redox conformation changes in refined tuna cytochrome c. Proc Nat Acad Sci USA 77:6371-6375.
74. Tanaka N, Yamane T, Tsukihara T, Ashida T, Kakudo M. 1975. The crystal structure of bonito (katsuo) ferrocytochrome c at 2.3 angstroms resolution. J Biochem (Tokyo) 77:147.
75. Tanaka T, Yamaguchi H, Kato H, Nishioka T, Katsube Y, Oda J. 1993. Flexibility impaired by mutations revealed the multifunctional roles of the loop in glutathione synthetase. Biochemistry 32:12398-12404.
76. Walker B, Krishnasastry M, Bayley H. 1993. Functional complementation of staphylococcal α-hemolysin fragments. Overlaps, nicks, and gaps in the glycine-rich loop. J Biol Chem 268:5285-5292.
77. Wolfson AJ, Kanaoka M, Lau FTK, Ringe D. 1991. Insertion of an elastase-binding loop into interleukin-1β. Protein Eng 4:313-317.